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Canine rabies virus variant has been eliminated in the United States and multiple other countries. Globally, however, dogs remain the principal source for human rabies infections (1). The World Health Organization recommends that when dogs cross international borders, national importing authorities should require an international veterinary certificate attesting that the animal did not show signs of rabies at the time of shipment, was permanently identified, vaccinated, or revaccinated, and had been subjected to a serologic test for rabies before shipment (1). On June 8, 2015, an adult female dog that had recently been picked up from the streets of Cairo, Egypt, and shipped by a U.S. animal rescue organization to the United States was confirmed to have rabies by the Virginia Department of General Services Division of Consolidated Laboratory Services (DCLS). This dog was part of a large shipment of dogs and cats from Egypt that rescue organizations had distributed to multiple states for adoption. During the investigation, public health officials learned that the rabies vaccination certificate used for entry of the rabid dog into the United States had intentionally been falsified to avoid exclusion of the dog from entry under CDC's current dog importation regulations. This report underscores the ongoing risk posed by U.S. importation of domestic animals that have not been adequately vaccinated against rabies.

Case Report

On May 30, 2015, a shipment of eight dogs and 27 cats arrived at John F. Kennedy International Airport in New York City from Cairo, Egypt. The animals were distributed to several animal rescue groups and one permanent adoptive home in New Jersey, Pennsylvania, Maryland, and Virginia. Four dogs from the shipment arrived in Virginia on May 31, 2015, and were distributed to three foster homes associated with a Virginia-based rescue group (animal rescue group A).

On June 3, an adult female street dog (dog A) imported by animal rescue group A became ill. The dog had been imported with an unhealed fracture of the left forelimb, and 4 days after arrival at a foster home in Virginia, developed hypersalivation, paralysis, and hyperesthesia. Because of concern about rabies, a veterinarian euthanized the dog on June 5 and submitted brain tissue for rabies testing at DCLS. On June 8, DCLS confirmed rabies infection by direct fluorescent antibody testing and contacted CDC to coordinate shipment of specimens to assist with variant typing. CDC determined that the variant was consistent with canine rabies virus circulating in Egypt.

Public Health Investigation

After DCLS confirmed the rabies diagnosis, the Virginia Department of Health, the New Jersey Department of Health, the New York City Department of Health and Mental Hygiene, and CDC initiated human and domestic animal rabies exposure assessments associated with the entire animal shipment. The infectious period for dog A was considered to have begun 10 days before symptom onset and continued until death (i.e., from May 24 to June 5) (2). The investigation also involved the Maryland Department of Health and Mental Hygiene, the Pennsylvania Department of Health, U.S. Customs and Border Protection, the foreign airline that transported the animals, the Egyptian Ministry of Health and Population, and the U.S. Department of Agriculture's Animal and Plant Health Inspection Service.

Potential human exposures were identified by interviewing U.S.-based airline cargo staff members, the U.S. transporter, dog A's caretaker, and volunteers and employees associated with animal rescue group A. Upon the shipment's arrival in New York, eight persons were involved in moving the dogs and cats from the plane onto a transport trailer and then into the U.S. transporter's vehicle. The New York City Department of Health and Mental Hygiene interviewed these eight persons; all reported having worn leather gloves while handling the crates and having had no direct contact with the animals. Public health investigators determined that the animals did not have contact with each other during transport except for dog A and her puppy aged 10 weeks (dog B), which were transported in the same crate. Both dogs had reportedly been collected off the streets of Cairo 5 days before shipment.

Among the eight dogs in the Egyptian shipment, only dog A and two dogs aged 6 months (dogs F and G) had certificates indicating rabies vaccination at or after age 3 months and ≥30 days before arrival at a U.S. port of entry (Table), as required by CDC dog importation regulations (3). Following dog A's rabies diagnosis, rescue workers reported that the dog's vaccination certificate had been intentionally predated in Egypt.

The Virginia investigation focused on contact with dog A after departing the airport cargo area through the time of the veterinary assessment in Virginia. Health department personnel in Virginia evaluated 30 persons for possible rabies exposure; no bite exposures were reported. Eighteen persons initiated rabies postexposure prophylaxis (PEP), including 10 who were considered to have been exposed and eight who requested PEP despite reporting no clear rabies exposure. Eight of the 18 persons receiving PEP reported having previously received rabies preexposure prophylaxis.

Domestic animal exposure investigations revealed that all animals in the Egyptian shipment, except for dogs A and B, had been crated individually in the airplane's cargo hold and held separately after arriving in the United States, until delivered to their final destinations. Investigators thought it unlikely that the cats in this shipment had interacted with dog A, even while in Egypt. CDC's cat importation regulations do not require that cats be vaccinated against rabies; therefore, the cats were not required under federal regulations to be confined, vaccinated, or revaccinated against rabies.

The Virginia Department of Health considered that the only dog among the animals in the Egyptian shipment to have been exposed to dog A during the rabies infectious period was her puppy, dog B. Dog A's caretaker was pet sitting a neighbor's dog and providing care within her household for eight other dogs, as well as nine other animals. The Virginia Department of Health identified seven dogs in dog A's caretaker's home as having been exposed to rabies. (Dog B was housed with a different caretaker.) The local health department determined that all of the exposed dogs except dog B had current rabies vaccination certificates from licensed veterinary hospitals. The dogs with current certificates received a rabies booster vaccination followed by 45 days of confinement at their owners' homes, as recommended by the Compendium of Animal Rabies Prevention and Control (4). Dog B, who was aged <12 weeks at the time and had not received an initial dose of rabies vaccine, was vaccinated against rabies and placed in strict isolation* for 90 days, followed by 90 days of home confinement (Table). To ensure that the dog was vaccinated according to the vaccine manufacturer's label specifications (at age ≥3 months), another dose of rabies vaccine was administered to dog B 1 month before release from strict isolation (Table). Dogs C and D each received a booster dose of rabies vaccine, followed by 90 days of home confinement.

The New Jersey Department of Health interviewed volunteers from a canine rescue group in New Jersey (animal rescue group B) that had received four of the eight dogs from the Egyptian shipment. All four dogs received either their initial rabies vaccination or a rabies booster vaccination and were ordered to be confined in their owners' homes for 6 months (Table).

Discussion

Rabies, the deadliest of all zoonotic diseases, accounts for an estimated 59,000 human deaths globally each year (5). The virus can infect any mammal, and once symptoms appear, the disease is almost invariably fatal (6). Importation of rabid animals into the United States has broad public health implications. The reintroduction of a canine rabies virus variant† or introduction of any nonendemic rabies viruses into a naïve animal population has the potential to change the epizootiology of rabies in the United States, leading to severe health consequences and economic losses (7).

To prevent human rabies exposures and introduction of rabies viruses, U.S. federal and state regulations place strict rabies vaccination requirements on dogs. Current CDC dog importation regulations require that dogs being imported from countries not considered rabies-free§ be accompanied by a valid rabies vaccination certificate (3). A valid rabies vaccination certificate documents a rabies vaccination for a dog aged ≥3 months that was administered ≥30 days before arrival in the United States (3). State regulations often are more strict. For example, all dogs and cats imported into Virginia by rescue groups must be accompanied by a Certificate of Veterinary Inspection issued by a veterinarian in the state or country of origin no fewer than 10 days before the animal enters Virginia. In addition, if the animal (i.e., a dog or cat) is aged ≥4 months, it must be vaccinated against rabies.

These importation regulations are difficult to enforce because of limited resources at U.S. ports of entry to inspect dog shipments. This report details the fourth known instance of a rabid dog imported from a non-U.S. territory since 2004 and the second instance of importation by a rescue organization of a rabid dog from the Middle East (4,8). However, other cases might have gone unreported because rabies can have a variable clinical course (4) that might not prompt animal owners or veterinarians to seek postmortem rabies testing.

CDC and state agencies have previously received reports of invalid or questionable health and rabies vaccination certificates for imported dogs (9); in at least one reported case, a veterinarian issued a Certificate of Veterinary Inspection for a dog that was already showing signs of rabies infection (10). CDC has attempted to address mounting concerns about importation of inadequately vaccinated dogs, either resulting from inaccurate rabies vaccination certificates or from legal importation under an existing mechanism allowing exceptions to CDC's regulatory requirement (i.e., issuance of a dog confinement agreement that serves as a legal and binding agreement between CDC and the importer and lists requirements for vaccination and confinement of the animal).

In May 2014, CDC issued the health alert notification "Imported Dogs with Questionable Documents" specifically because of ongoing concerns with dogs' entry documents listing incorrect ages and rabies vaccination status. In addition, in July 2014, CDC published the notice "Issuance and Enforcement Guidance for Dog Confinement Agreements"¶ in the Federal Register clarifying that entry into the United States of dogs that are inadequately vaccinated against rabies and coming from countries where rabies is endemic would only be allowed on a limited and case-by-case basis. In the incident described in this report, under the criteria outlined in the Federal Register notice, CDC would ordinarily have excluded five of the eight dogs in the shipment (dogs B, C, D, E, and H). However, CDC was not notified of the arrival of these dogs until after the dogs had already been admitted into the United States and left the port of entry. Because dog A was accompanied by a rabies vaccination certificate that only later was reported to have been falsified, CDC would most likely have admitted dog A.

This report underscores the current difficulties in verifying any imported dog's rabies vaccination certificate and health status. The United States also is vulnerable to an increasing risk for rabies introduction and spread from other imported domestic animals, such as cats and ferrets. Considering the public health risk posed by importation of animals for the purposes of placing them in adoptive homes in the United States, and the current oversupply of adoptable animals already in the United States, persons and organizations involved with importing pets for the purposes of adoption should consider reevaluating, and potentially redirecting, their current efforts. Globally, animal welfare stakeholders should consider focusing their efforts on supporting local organizations that provide adoptive homes, along with health care services, for street animals in their own countries. In addition, although this report focuses on imported dogs and rabies, all animals pose a risk for transmission of zoonotic diseases (e.g., brucellosis, leishmaniasis, campylobacteriosis, leptospirosis, giardiasis, and cutaneous or visceral larva migrans). Documentation of overall health status, not just rabies vaccination, is critical to minimizing the risk from importing animals carrying zoonotic diseases.

1Division of Global Migration and Quarantine, National Center for Emerging and Zoonotic Infectious Diseases, CDC; 2Division of High-Consequence Pathogens and Pathology, National Center for Emerging and Zoonotic Infectious Diseases, CDC; 3Virginia Department of Health; 4Virginia Department of General Services Division of Consolidated Laboratory Services; 5New Jersey Department of Health; 6New York City Department of Health and Mental Hygiene.

* Isolation in this context refers to confinement in an enclosure that precludes direct contact with humans and other animals. In Virginia, this means that an animal is placed in a double walled enclosure that allows for feeding, watering, cleaning, and general care but will not allow for any person or other domestic animal to have contact with the isolated animal.

† In this incident, the phylogenetic reconstruction based on the complete nucleoprotein gene is closely related to a canine rabies virus variant circulating in domestic dogs in Egypt (Africa 4 clade).

Canine rabies virus variant has been eliminated from the United States. Rabies vaccination programs in the United States have eliminated domestic dogs as a reservoir of rabies. In contrast, domestic dogs worldwide continue to pose the greatest threat for rabies transmission to humans.

What is added by this report?

Importations of dogs, and potentially other domestic animals that are inadequately vaccinated against rabies, from countries where rabies is endemic continues to present a risk to an unaware U.S. public. Officials, veterinarians, and caretakers might be unable to verify the validity of rabies vaccination certificates issued before an animal's importation.

What are the implications for public health practice?

To eliminate domestic dogs as the principal source for rabies transmission to humans, efforts need to focus on rabies elimination programs worldwide. Domestic animals moving across borders should be adequately protected against and screened for rabies infections.

TABLE. Age and reported rabies vaccination or revaccination dates for eight dogs shipped from Egypt to the United States on May 30, 2015

Dog

Information provided on Egyptian rabies vaccination certificate

Vaccination or revaccination after arrival in the United States

Age or date of birth

Date of rabies vaccination

Final U.S. destination

Date of U.S. rabies vaccination or revaccination

End of confinement period*

A

2 yrs

April 25, 2015

Virginia

Not applicable

Not applicable

B

10 wks

Not vaccinated

Virginia

June 9, 2015 and July 31, 2015

September 1, 2015† and November 30, 2015

C

4 mos

May 24, 2015

Virginia

June 11, 2015

September 9, 2015

D

4 mos

May 24, 2015

Virginia

June 11, 2015

September 9, 2015

E

01/15/2015

Unknown

New Jersey

June 13, 2015

November 30, 2015

F

6 mos

April 5, 2015

New Jersey

June 13, 2015

November 30, 2015

G

6 mos

April 6, 2015

New Jersey

June 13, 2015

November 30, 2015

H

2013

Unknown

New Jersey

June 13, 2015

November 30, 2015

* Includes CDC confinement period of 30 days following initial vaccination or revaccination against rabies. Rabies postexposure quarantine regulations vary among states.

† Initial 90-day period, when dog B was in strict isolation.

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